Evolution of flavors and scents

Annual Review of Plant Biology

Volumn 56, Issue , 2005, Pages 301-325

  Gang, David R ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Acyltransferases; O methyltransferases; Repeated evolution; Specialized metabolism; Terpene synthases; Volatile emission

Indexed keywords

FLAVORING AGENT;

ENZYMOLOGY; EVOLUTION; METABOLISM; ODOR; PLANT; REVIEW; VOLATILIZATION;

EVOLUTION; FLAVORING AGENTS; ODORS; PLANTS; VOLATILIZATION;

CLARKIA; CLARKIA BREWERI; OCIMUM BASILICUM; ROSA;

EID: 20444385145     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.56.032604.144128     Document Type: Review

References (100)

1. Adams S, Weidenborner M. 1996. Mycelial deformations of Cladosporium herbarum due to the application of eugenol or carvacrol. J. Essent. Oil. Res. 8:535-40
2. Aharoni A, Keizer LCP, Bouwmeester HJ, Sun ZK, Alvarez-Huerta M, et al. 2000. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12:647-61
3. Aubourg S, Lecharny A, Bohlmann J. 2002. Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol. Gen. Genomics 267:730-45
4. Back K, Chappell J. 1995. Cloning and bacterial expression of a sesquiterpene cyclase from Hyoscyamus muticus and its molecular comparison to related terpene cyclases. J. Biol. Chem. 270:7375-81
5. Bender J. 2004. DNA methylation and epigenetics. Ann. Rev. Plant Biol. 55:41-68
6. Boatright J, Negre F, Chen X, Kish CM, Wood B, et al. 2004. Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol. 135:1993-2011
7. Bohlmann J, Martin D, Oldham NJ, Gershenzon J. 2000. Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-β-ocimene synthase. Arch. Biochem. Biophys. 375:261-69
8. Bohlmann J, Meyer-Gauen G, Croteau R. 1998. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc. Nat. Acad. Sci. USA 95:4126-33
9. Bood KG, Zabetakis I. 2002. The biosynthesis of strawberry flavor (II): biosynthetic and molecular biology studies. J. Food Sci. 67:2-8
10. Bullerman LB, Lieu FY, Seier SA. 1977. Inhibition of growth and aflatoxin production by cinnamon and clove oils. J. Food Sci. 42:1107-9, 16
11. Chandler VL, Stam M. 2004. Chromatin conversations: mechanisms and implications of paramutation. Nat. Rev. Genet. 5:532-44
12. Chandler VL, StamM, Sidorenko LV. 2002. Long-distance cis and trans interactions mediate paramutation. Adv. Med. Incorp. Molec. Genet. Med. 46:215-42
13. Chen F, Ro D-K, Petri J, GershenzonJ, Bohlmann J, et al. 2004. Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiol. 135:1956-66
14. Chen F, Tholl D, D'Auria JC, Farooq A, Pichersky E, Gershenzon J. 2003. Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell 15:481-94
15. Chen SX, Glawischnig E, Jorgensen K, Naur P, Jorgensen B, et al. 2003. CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J. 33:923-37
16. Chen XY, Chen Y, Heinstein P, Davisson VJ. 1995. Cloning, expression, and characterization of (+)-delta-cadinene synthase: a catalyst for cotton phytoalexin biosynthesis. Arch. Biochem. Biophys. 324:255-66
17. Chen XY, Wang MS, Chen Y, Davisson VJ, Heinstein P. 1996. Cloning and heterologous expression of a second (+)-delta-cadinene synthase from Gossypium arboreum. J. Nat. Prod. 59:944-51
18. Colby S, Crock J, Dowdle-Rizzo B, Lemaux P, Croteau R. 1998. Germacrene C synthase from Lycopersicon esculentum cv. VFNT cherry tomato: cDNA isolation, characterization, and bacterial expression of the multiple product sesquiterpene cyclase. Proc. Nat. Acad. Sci. USA 95:2216-21
19. Crowell AL, Williams DC, Davis EM, Wildung MR, Croteau R. 2002. Molecular cloning and characterization of a new linalool synthase. Arch. Biochem. Biophys. 405:112-21
20. Cseke L, Dudareva N, Pichersky E. 1998. Structure and evolution of linalool synthase. Mol. Biol. Evol. 15:1491-98
21. D'Auria JC, Chen F, Pichersky E. 2002. Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiol. 130:466-76
22. Davies KM, Schwinn KE. 2003. Transcriptional regulation of secondary metabolism. Funct. Plant Biol. 30:913-25
23. Dobson HEM, Bergstrom G. 2000. The ecology and evolution of pollen odors. Plant Syst. Evol. 222:63-87
24. Dobson HEM, Groth I, Bergstrom G. 1996. Pollen advertisement: chemical contrasts between whole-flower and pollen odors. Am. J. Bot. 83:877-85
25. Dudareva N, Cseke L, Blanc VM, Pichersky E. 1996. Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell 8:1137-48
26. Dudareva N, D'Auria JC, Nam KH, Raguso RA, Pichersky E. 1998. Acetyl-CoA:benzylalcohol acetyltransferase - an enzyme involved in floral scent production in Clarkia breweri. Plant J. 14:297-304
27. Dudareva N, Pichersky E, Gershenzon J. 2004. Biochemistry of plant volatiles. Plant Physiol. 135:1893-902
28. Facchini PJ, Chappell J. 1992. Gene family for an elicitor-induced sesquiterpene cyclase in tobacco. Proc. Nat. Acad. Sci. USA 89:11088-92
29. Flament I, Debonneville C, Furrer A. 1993. Volatile constituents of roses. In Bioactive Volatile Compounds from Plants, ed. R Teranishi, R Buttery, H Sugisawa, pp. 269-81. Washington, DC: Am. Chem. Soc.
30. Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C. 2002. Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 30:47-59
31. Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, et al. 2002. The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J. 30:33-45
32. Fujita M, Gang DR, Davin LB, Lewis NG. 1999. Recombinant pinoresinol-lariciresinol reductases from western red cedar (Thuja plicata) catalyze opposite enantiospecific conversions. J. Biol. Chem. 274:618-27
33. Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E. 2002. Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol. 130:1536-44
34. Gang DR, Dinkova-Kostova AT, Davin LB, Lewis NG. 1997. Phylogenetic links in plant defense systems: lignans, isoflavonoids and their reductases. ACS Symp. Ser. 658:58-89
35. Gang DR, Lavid N, Zubieta C, Chen F, Beuerle T, et al. 2002. Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. Plant Cell 14:505-19
36. Gang DR, Simon J, Lewinsohn E, Pichersky E. 2002. Peltate glandular trichomes of Ocimum basilicum L. (Sweet Basil) contain high levels of enzymes involved in the biosynthesis of phenylpropenes. J. Herbs Spices Med. Plants 9:189-95
37. Gang DR, Wang J, Dudareva N, Nam KH, Simon JE, et al. 2001. An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol. 125:539-55
38. Gershenzon J, Maffei M, Croteau R. 1989. Biochemical and histochemical localization of monoterpene biosynthesis in the glandular trichomes of spearmint (Mentha spicata). Plant Physiol. 89:1351-57
39. Gershenzon J, McCaskill D, Rajaonarivony JIM, Mihaliak C, Karp F, Croteau R. 1992. Isolation of secretory cells from plant glandular trichomes and their use in biosynthetic studies of monoterpenes and other gland products. Anal. Biochem. 200:130-38
40. Goodwin SM, Kolosova N, Kish CM, Wood KV, Dudareva N, Jenks MA. 2003. Cuticle characteristics and volatile emissions of petals in Antirrhinum majus. Physiol. Plant. 117:435-43
41. Grammer K, Fink B, Moller AP, Thornhill R. 2003. Darwinian aesthetics: sexual selection and the biology of beauty. Biol. Rev. 78:385-407
42. Grayer R, Kite G, Goldstone F, Bryan S, Paton S, Putievsky E. 1996. Infraspecific taxonomy and essential oil chemotypes in sweet basil, Ocimum basilicum. Phytochemistry 43:1033-39
43. Grossman J. 1993. Botanical pesticides in Africa. IPM Pract. 15:1-9
44. Gupta S. 1994. Genetic analysis of some chemotypes in Ocimum basilicum var. glabratum. Plant Breed. 112:135-40
45. Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, et al. 2002. Rose scent: genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14:2325-38
46. Halkier BA, Hansen CH, Mikkelsen MD, Naur P, Wittstock U. 2002. The role of cytochromes P450 in biosynthesis and evolution of glucosinolates. Recent Adv. Phytochem. 36:223-48
47. Harrewijn P, Minks AK, Mollema C. 1995. Evolution of plant volatile production in insect-plant relationships. Chemoecology 5/6:55-73
48. Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, et al. 2004. Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell 16:1446-65
49. Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M. 2003. Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J. Biol. Chem. 278:95-103
50. Ibrahim RK, Muzac I. 2000. The methyltransferase gene superfamily: a tree with multiple branches. Recent Adv. Phytochem. 34:349-84
51. Iijima Y, Gang DR, Fridman E, Lewinsohn E, Pichersky E. 2004. Characterization of geraniol synthase from the peltate glands of sweet basil. Plant Physiol. 134:370-79
52. Jia JW, Crock J, Lu S, Croteau R, Chen XY. 1999. (3,R)-linalool synthase from Artemisia annua L.: cDNA isolation, characterization, and wound induction. Arch. Biochem. Biophys. 372:143-49
53. Kahn RA, Durst F. 2000. Function and evolution of plant cytochrome P450. Recent Adv. Phytochem. 34:151-89
54. Kaori S, Maeda T, Arimura G, Ozawa R, Shimoda T, Takabayashi J. 2002. Functions of plant infochemicals in tritrophic interactions between plants, herbivores and carnivorous natural enemies. Jap. J. Appl. Entomol. Zool. 46:117-33
55. Karapinar M, Aktug S. 1987. Inhibition of foodborne pathogens by thymol, eugenol, menthol and anethole. Int. J. Food Micro. 4:161-66
56. Kerschen A, Napoli CA, Jorgensen RA, Muller AE. 2004. Effectiveness of RNA interference in transgenic plants. FEBS Lett. 566:223-28
57. Kunst L, Samuels AL. 2003. Biosynthesis and secretion of plant cuticular wax. Prog. Lipid Res. 42:51-80
58. Lange BM, Ghassemian M. 2003. Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol. Biol. 51:925-48
59. Lavid N, Wang J, Shalit M, Guterman I, Bar E, et al. 2002. O-methyltransferases involved in the biosynthesis of volatile phenolic derivatives in rose petals. Plant Physiol. 129:1899-907
60. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, et al. 2002. Multifunctionality of plant ABC transporters - more than just detoxifiers. Planta 214:345-55
61. McCaskill D, Gershenzon J, Croteau R. 1992. Morphology and monoterpene biosynthetic capabilities of secretory cell clusters isolated from glandular trichomes of peppermint (Mentha piperita L.). Planta 187:445-54
62. Morales MR, Simon JE. 1997. 'Sweet Dani': a new culinary and ornamental lemon basil. Hortscience 32:148-49
63. Nam KH, Dudareva N, Pichersky E. 1999. Characterization of benzylalcohol acetyltransferases in scented and non-scented Clarkia species. Plant Cell Physiol. 40:916-23
64. Naur P, Petersen BL, Mikkelsen MD, Bak S, Rasmussen H, et al. 2003. CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol. 133:63-72
65. Noel JD, Dixon RA, Pichersky E, Zubieta C, Ferrer J. 2003. Structural, functional, and evolutionary basis for methylation of plant small molecules. In Recent Advances in Phytochemistry (Integrative Phytochemistry: From Ethnobotany to Molecular Ecology), ed. J Romeo, pp. 37-58. Oxford: Elsevier
66. Obeng-Ofori D, Reichmuth C. 1997. Bioactivity of eugenol, a major component of essential oil of Ocimum suave (Wild.) against four species of stored-product Coleoptera. Int. J. Pest. Manag. 43:89-94
67. Ober D, Hartmann T. 1999. Homospermidine synthase, the first pathway-specific enzyme of pyrrolizidine alkaloid biosynthesis, evolved from deoxyhypusine synthase. Proc. Nat. Acad. Sci. USA 96:14777-82
68. Perrière G, Gouy M. 1996. WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78:364-69
69. Pichersky E, Dudareva N, Wang J, Cseke L, Lewinsohn E. 1999. Biosynthesis of scent and flavor compounds. Curr. Plant Sci. Biotech. Agric. 36:601-4
70. Pichersky E, Gang DR. 2000. Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5:439-45
71. Piechulla B, Pott MB. 2003. Plant scents - mediators of inter- and intraorganismic communication. Planta 217:687-89
72. Qi X, Bakht S, Leggett M, Maxwell C, Melton R, Osbourn A. 2004. A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Nat. Acad. Sci. USA 101:8233-38
73. Raguso RA, Pichersky E. 1995. Floral volatiles from Clarkia breweri and C. concinna (Onagraceae): recent evolution of floral scent and moth pollination. Plant Syst. Evol. 194:55-67
74. Scalliet G, Journot N, Jullien F, Baudino S, Magnard JL, et al. 2002. Biosynthesis of the major scent components 3,5-dimethoxytoluene and 1,3,5-trimethoxybenzene by novel rose O-methyltransferases. FEBS Lett. 523:113-18
75. Schiestl FP, Ayasse M. 2002. Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Syst. Evol. 234:111-19
76. Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, et al. 2001. CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 276:36566-74
77. Schuler MA. 1996. Plant cytochrome P450 monooxygenases. Crit. Rev. Plant Sci. 15:235-84
78. Evans GB, ed. 1974. The Tragedy of Romeo and Juliet, Act II, Scene II, Lines 43-44. In The Riverside Shakespeare, pp. 1058-99. Boston: Houghton Mifflin
79. Shalit M, Guterman I, Volpin H, Bar E, Tamari T, et al. 2003. Volatile ester formation in roses. Identification of an acetyl-coenzyme A: geraniol/citronellol acetyltransferase in developing rose petals. Plant Physiol. 131:1868-76
80. Sisk C, Shorey H, Gerber R, Gaston L. 1996. Semiochemicals that disrupt foraging by the Argentine ant (Hymenoptera: Formicidae): laboratory bioassays. J. Econ. Entom. 89:381-85
81. St-Pierre B, De Luca V. 2000. Evolution of acyltransferase genes: origin and diversification of the BAHD superfamily of acyltransferases involved in secondary metabolism. Recent Adv. Phytochem. 34:285-315
82. Stam M, Belele C, Dorweiler JE, Chandler VL. 2002. Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 16:1906-18
83. Steeghs M, Bais HP, Gouw JD, Goldan P, Kuster W, et al. 2004. Proton-transfer-reaction mass spectrometry as a new tool for real time analysis of root-secreted volatile organic compounds in Arabidopsis. Plant Physiol. 135:47-58
84. Takeshita N, Fujiwara H, Mimura H, Fitchen JH, Yamada Y, Sato F. 1995. Molecular-cloning and characterization of 5-adenosyl-L-methionine-scoulerine-9- O-methyltransferase from cultured cells of Coptis japonica. Plant Cell Physiol. 36:29-36
85. Tamura K. 1999. TreeExplorer. TMU Evolutionary Genetics Laboratory. (http://evolgen. biol.metro-u.ac.jp/TE/TE_man.html)
86. Theis N, Lerdau M. 2003. The evolution of function in plant secondary metabolites. Int. J. Plant Sci. 164:S93-S102
87. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuclic Acids Res. 25:4876-82
88. Trapp SC, Croteau RB. 2001. Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811-32
89. Verlet N. 1993. Commercial aspects. In Volatile Crops: Their Biology, Biochemistry and Production, ed. RKM Hay, PG Waterman, pp. 137-74. Essex, England: Longman Scientific & Technical
90. Vinson SB. 1999. Parasitoid manipulation as a plant defense strategy. Annals Entomol. Soc. Am. 92:812-28
91. Vogt T. 2000. Glycosyltransferases involved in plant secondary metabolism. Recent Adv. Phytochem. 34:317-47
92. Wang J, Pichersky E. 1998. Characterization of S-adenosyl-L-methionine: (iso)eugenol O-methyltransferase involved in floral scent production in Clarkia breweri. Arch. Biochem. Biophys. 349:153-60
93. Wang J, Pichersky E. 1999. Identification of specific residues involved in substrate discrimination in two plant O-methyltransferases. Arch. Biochem. Biophys. 368:172-80
94. Watanabe N, Washio H, Straubinger M, Knapp H, Winterhalter P. 1998. Occurrence of a glucosidic progenitor of rose oxide in rose flowers, Rosa damascena Mill. Nat. Prod. Lett. 12:5-10
95. Watanabe S, Hayashi K, Yagi K, Asai T, MacTavish H, et al. 2002. Biogenesis of 2-phenylethanol in rose flowers: incorporation of H-2(8) L-phenylalanine into 2-phenylethanol and its beta-D-glucopyranoside during the flower opening of Rosa 'Hoh-Jun' and Rosa damascena Mill. Biosci. Biotech. Biochem. 66:943-47
96. Wein M, Lavid N, Lunkenbein S, Lewinsohn E, Schwab W, Kaldenhoff R. 2002. Isolation, cloning and expression of a multifunctional O-methyltransferase capable of forming 2,5-dimethyl-4-methoxy-3(2H)-furanone, one of the key aroma compounds in strawberry fruits. Plant J. 31:755-65
97. Wink M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3-19
98. Wink M, Mohamed GIA. 2003. Evolution of chemical defense traits in the Leguminosae: mapping of distribution patterns of secondary metabolites on a molecular phylogeny inferred from nucleotide sequences of the rbcL gene. Biochem. Syst. Ecol. 31:897-917
99. Wu SQ, Watanabe N, Mita S, Dohra H, Ueda Y, et al. 2004. The key role of phloroglucinol O-methyltransferase in the biosynthesis of Rosa chinensis volatile 1,3,5-trimethoxybenzene. Plant Physiol. 135:95-102
100. Wu SQ, Watanabe N, Mita S, Ueda Y, Shibuya M, Ebizuka Y. 2003. Two O-methyltransferases isolated from flower petals of Rosa chinensis var. spontanea involved in scent biosynthesis. J. Biosci. Bioeng. 96:119-28